Cultural differences in anterior cingulate cortical response to prediction error

Roles of the medial frontal cortices in the selection, storage and retrieval of response tactics in a voluntary arm-reaching task

Inhibitory control is a key executive function and has been studied extensively using the stop signal task. By applying a simple race model that posits an independent race between a GO process responsible for initiation of responses and a STOP process responsible for inhibition of responses, one can estimate how long it takes an individual to inhibit an ongoing response, the stop signal reaction time. Here, we examined how stop signal reaction time can be affected by working memory. Participants engaged in a dual task; they completed a stop signal task under low and high working memory load conditions. Working memory capacity was also measured. We found that the STOP process was lengthened in the high, compared to the low, working memory load condition, as evidenced by differences in stop signal reaction time. The GO process was unaffected and working memory capacity could not account for differences across the load conditions. These results indicate that inhibitory control can be influenced by placing demands on working memory.

Event Abstract Back to Event Brain pathways underlying Response Inhibition and Response Caution Renate Thienel1*, Elise Mansfield1, Patrick S. Cooper1, Andrew Heathcote1, Birte Forstmann2, Pat Michie1, Gavin Cooper1 and Frini Karayanidis1 1 School of Psychology, University of Newcastle, Australia 2 University of Amsterdam, Netherlands Background: Our previous findings suggest that the striatum is instrumental in mediating response caution in a task switching paradigm (Mansfield et al., J. Neurosci 2011, 31:14688-92), and that structural integrity in two separate fronto-striatal networks are associated with adopting an overall more risky or more cautious response threshold. In the present study, we examine whether a similar network underlies response inhibition, as operationalized by a stop signal task. Response inhibition has been shown to be mediated by cortical and subcortical structures within the inferior frontal lobe and the subthalamic nucleus, respectively. We investigate whether structural integrity measures in these regions can explain the relationship between stop signal related event related potential (ERP) components and estimates of stop signal reaction time (SSRT). Finally the relationship between, and the differential structural pathways contributing to, response threshold adjustment (task-switching paradigm) and stop signal response time will be examined. Methods: Diffusion weighted Imaging (DWI), ERP and behavioural data has been collected in 16 healthy participants (24.5 years, 5 male). A correlational analysis was performed for the ERPs and the behavioural measures of both tasks (task switching and stop signal task). Tract based spatial statistics (TBSS) of the DWI data was performed to compare the white matter pathways associated with response thresholds adjustment (task-switching task), and response inhibition (stop-signal task) respectively. These regions were then used to explain variation in ERP data. Results/Discussion: The integrity within distinct structural pathways (DWI data) explained the relationship between (1) ERP measures and response threshold adjustment and (2) ERP measures and SSRTs. Distinct fronto-basal ganglia pathways mediated threshold setting and response suppression. Keywords: task-switching, stop signal task, DWI, fronto-striatal circuits, response inhibition Conference: ACNS-2013 Australasian Cognitive Neuroscience Society Conference, Clayton, Melbourne, Australia, 28 Nov - 1 Dec, 2013. Presentation Type: Poster Topic: Executive Processes Citation: Thienel R, Mansfield E, Cooper PS, Heathcote A, Forstmann B, Michie P, Cooper G and Karayanidis F (2013). Brain pathways underlying Response Inhibition and Response Caution. Conference Abstract: ACNS-2013 Australasian Cognitive Neuroscience Society Conference. doi: 10.3389/conf.fnhum.2013.212.00145 Copyright: The abstracts in this collection have not been subject to any Frontiers peer review or checks, and are not endorsed by Frontiers. They are made available through the Frontiers publishing platform as a service to conference organizers and presenters. The copyright in the individual abstracts is owned by the author of each abstract or his/her employer unless otherwise stated. Each abstract, as well as the collection of abstracts, are published under a Creative Commons CC-BY 4.0 (attribution) licence (https://creativecommons.org/licenses/by/4.0/) and may thus be reproduced, translated, adapted and be the subject of derivative works provided the authors and Frontiers are attributed. For Frontiers’ terms and conditions please see https://www.frontiersin.org/legal/terms-and-conditions. Received: 25 Sep 2013; Published Online: 25 Nov 2013. * Correspondence: Dr. Renate Thienel, School of Psychology, University of Newcastle, Newcastle, Australia, renate.thienel@newcastle.edu.au Login Required This action requires you to be registered with Frontiers and logged in. To register or login click here. Abstract Info Abstract The Authors in Frontiers Renate Thienel Elise Mansfield Patrick S Cooper Andrew Heathcote Birte Forstmann Pat Michie Gavin Cooper Frini Karayanidis Google Renate Thienel Elise Mansfield Patrick S Cooper Andrew Heathcote Birte Forstmann Pat Michie Gavin Cooper Frini Karayanidis Google Scholar Renate Thienel Elise Mansfield Patrick S Cooper Andrew Heathcote Birte Forstmann Pat Michie Gavin Cooper Frini Karayanidis PubMed Renate Thienel Elise Mansfield Patrick S Cooper Andrew Heathcote Birte Forstmann Pat Michie Gavin Cooper Frini Karayanidis Related Article in Frontiers Google Scholar PubMed Abstract Close Back to top Javascript is disabled. Please enable Javascript in your browser settings in order to see all the content on this page.

BackgroundA robust feature of sensorimotor synchronization (SMS) performance in finger tapping to an auditory pacing signal is the negative asynchrony of the tap with respect to the pacing signal. The Paillard–Fraisse hypothesis suggests that negative asynchrony is a result of inter-modal integration, in which the brain compares sensory information across two modalities (auditory and tactile). The current study compared the asynchronies of vocalizations and finger tapping in time to an auditory pacing signal. Our first hypothesis was that vocalizations have less negative asynchrony compared to finger tapping due to the requirement for sensory integration within only a single (auditory) modality (intra-modal integration). However, due to the different measurements for vocalizations and finger responses, interpreting the comparison between these two response modalities is problematic. To address this problem, we included stop signals in the synchronization task. The rationale for this manipulation was that stop signals would perturb synchronization more in the inter-modal compared to the intra-modal task. We hypothesized that the inclusion of stop signals induce proactive inhibition, which reduces negative asynchrony. We further hypothesized that any reduction in negative asynchrony occurs to a lesser degree for vocalization than for finger tapping.MethodA total of 30 participants took part in this study. We compared SMS in a single sensory modality (vocalizations (or auditory) to auditory pacing signal) to a dual sensory modality (fingers (or tactile) to auditory pacing signal). The task was combined with a stop signal task in which stop signals were relevant in some blocks and irrelevant in others. Response-to-pacing signal asynchronies and stop signal reaction times were compared across modalities and across the two types of stop signal blocks.ResultsIn the blocks where stopping was irrelevant, we found that vocalization (−61.47 ms) was more synchronous with the auditory pacing signal compared to finger tapping (−128.29 ms). In the blocks where stopping was relevant, stop signals induced proactive inhibition, shifting the response times later. However, proactive inhibition (26.11 ms) was less evident for vocalizations compared to finger tapping (58.06 ms).DiscussionThese results support the interpretation that relatively large negative asynchrony in finger tapping is a consequence of inter-modal integration, whereas smaller asynchrony is associated with intra-modal integration. This study also supports the interpretation that intra-modal integration is more sensitive to synchronization discrepancies compared to inter-modal integration.

Conflict anticipation in alcohol dependence — A model-based fMRI study of stop signal task

The Stop Signal Task (SST), a commonly used measure of response inhibition, uses standard psychophysical methods to gain an estimate of the time needed to withhold a prepotent response. Under some circumstances, conventional forms of the SST are impractical to use because of the large number of trials necessary to gain a reliable estimate of the speed of inhibition. Here we applied to the SST an adaptive method for estimating psychometric parameters that can find reliable threshold estimates over a relatively small number of trials. The Ψ adaptive staircase, which uses a Bayesian algorithm to find the most likely parameters of a psychophysical function, was used to estimate the critical stop signal delay at which the probability of successful response inhibition equals 0.5. Using computational modeling and adult participants, estimates of stop signal reaction time (SSRT) based on the Ψ staircase were compared to estimates using the method of constant stimuli and a standard staircase method of adjustment. Results demonstrate that a reliable estimate of SSRT can be gained very quickly (20–30 stop trials), making the method very useful for testing populations that cannot maintain concentration for long periods or for rapidly obtaining multiple SSRT estimates from healthy adult participants.

The ability to inhibit actions inappropriate for the context is essential for meeting the shifting demands of complex environments. The stop signal task (SST) has been used in many previous studies to examine the interactions between go and stop responses in a cognitively demanding task involving attention, conflict resolution, and motor plan selection. The current study uses a variant of the SST, in which the continue signal instructs participants to proceed with the go response they were preparing. Reaction times (RTs) on continue trials were bimodally distributed, suggesting that an aspect of inhibition was involved in at least some of the trials. We investigated whether the cognitive processes delaying the generation of a behavioural response on continue trials are the same as for stop trials. We found improvement of stop signal reaction times (SSRTs) following stop trials, but the decrease in continue signal reaction times (CSRTs) was not significant. No improvement in either SSRT or CSRT was found following continue trials, suggesting that activation of the processes delaying the response on continue trials is insufficient to drive subsequent adjustments in SSRT or CSRT. In addition, go RTs only slowed following stop trials. These effects may suggest the presence of a selective learning process, which requires that the initial inhibition captured by SSRT and CSRT be combined with recognition of the stop signal specifically to affect subsequent performance.

BackgroundAltered brain activity that has been observed in attention deficit hyperactivity disorder (ADHD) while performing cognitive control tasks like the stop signal task (SST) has generally been interpreted as reflecting either weak (under-active) or compensatory (over-active) versions of the same functions as in healthy controls. If so, then regional activities that correlate with the efficiency of inhibitory control (i.e. stop signal reaction time, SSRT) in healthy subjects should also correlate with SSRT in ADHD. Here we test the alternate hypothesis that BOLD (blood-oxygen-level-dependent) differences might instead reflect the redirection of neural processing resources normally used for task-directed inhibitory control, towards actively managing symptomatic behaviour. If so, then activities that correlate with SSRT in TD should instead correlate with inattentive and hyperactive symptoms in ADHD.MethodsWe used fMRI (functional magnetic resonance imaging) in 14 typically developing (TD) and 14 ADHD adolescents performing the SST, and in a replication sample of 14 healthy adults. First, we identified significant group BOLD differences during all phases of activity in the SST (i.e. warning, response, reactive inhibition, error detection and post-error slowing). Next, we correlated these phases of activity with SSRT in TD and with SSRT, inattentive and hyperactive symptom scores in ADHD. We then identified whole brain significant correlations in regions of significant group difference in activity.ResultsOnly three regions of significant group difference were correlated with SSRT in TD and replication groups (left and right inferior frontal gyri (IFG) during error detection and hypothalamus during post-error slowing). Consistent with regions of altered activity managing symptomatic behaviour instead of task-directed behaviour, left IFG correlated with greater inattentive score, right IFG correlated with lower hyperactive score and hypothalamus correlated with greater inattentive score and oppositely correlated with SSRT compared to TD.ConclusionsStimuli that elicit task-directed integration of neural processing in healthy subjects instead appear to be directing integrated function towards managing symptomatic behaviour in ADHD. The ability of the current approach to determine whether altered neural activities reflect comparable functions in ADHD and control groups has broad implications for the development and monitoring of therapeutic interventions.

According to the balance model of self-regulation, dysfunction of the inhibitory control and reward processing might be a behavioral marker for addiction and problematic behaviors. Although several studies have separately examined the inhibitory control or reward processing of individuals exhibiting problematic Internet use (PIU), no study has explored these two functions simultaneously to examine the potential imbalance of these functions. This study aimed to investigate whether the self-regulatory failure of PIU individuals results from deficits in both inhibitory control [indexed with the stop signal reaction time (SSRT) in a stop signal task] and risk taking with losses (measured as the acceptance rates of risky gables or the ratio of win/loss in a mixed gambles task). The results revealed that PIU individuals, compared with controls, showed decreased SSRT and increased error rates as well as reduced risk taking with losses. Correlational analyses revealed a significant positive relationship between the SSRT and risk taking with losses. These findings suggest that both the inhibitory control and reward functions are impaired in PIU individuals and reveal an association between these two systems. These results strengthen the balance model of self-regulation theory’s argument that deficits in inhibitory control and risk taking with losses may assist in identifying risk markers for early diagnosis, progression, and prediction of PIU.

The aim of this work is to further understanding into the biological bases of human executive control through an integration of neuropsychology,psychopharmacology and functional imaging. Executive control includes the prototypical executive functions of response inhibition and error awareness. Response inhibition can be further divided into action cancellation and action restraint, which were assayed with the stop signal (SST) and Error Awareness(EAT) tasks, respectively. The EAT, which is a modified go-no go paradigm, was also used to measure error awareness behaviour. Monoamine neurotransmitters, specifically dopamine, noradrenaline and serotonin, were modulated during task performance with acute doses of methylphenidate (a dopamine and noradrenaline reuptake inhibitor), atomoxetine (a noradrenaline reuptake inhibitor), citalopram (a serotonin reuptake inhibitor) and cabergoline (a D2 agonist). The pharmacoimaging correlates of task performance were also examined with functional magnetic resonance imaging (fMRI). All experiments adhered to a randomised, double blind, placebo-controlled, crossover design and were limited to 18-35 year old healthy right-handed male participants. In Chapter 1, twenty-four (24) participants received acute doses of methylphenidate (30mg), atomoxetine (60mg), citalopram (30mg) and placebo and performed the SST. Methylphenidate, but not atomoxetine or citalopram, led to a reduction in response time variability and stop-signal reaction time indicating enhanced action cancellation compared with the other drug conditions. This enhancement occurred without change to overall response speed suggesting that methylphenidate was modulating core response inhibition processes rather than simply augmenting overall processing speed. This result argued for the prominence of dopaminergic, rather than adrenergic or serotonergic, mechanisms in action cancellation. In Chapter 2, the pharmacoimaging correlates of action restraint aspect were explored. Twenty-seven (27) males received acute doses of methylphenidate(30mg), atomoxetine (60mg), citalopram (30mg) and placebo whilst undertaking the EAT during fMRI. No-go related BOLD activations were then correlated for each of the drug conditions. Although Inhibitory performance under methylphenidate was numerically superior to the other drug conditions,this difference did not achieve statistical significance. On fMRI, methylphenidate activated, versus placebo, the anterior cingulate cortex, right inferior frontal, left middle frontal, left angular and right superior temporal gyri and right caudate. Atomoxetine activated a broad network of cortical regions. Both methylphenidate and atomoxetine, but not citalopram, activated superior temporal, right inferior frontal and left middle frontal clusters. Citalopram only activated the left inferior occipital lobe. Taking each condition’s activations as functionally defined regions of interest, the specificity of no-go related activity was compared across the four conditions. Only methylphenidate demonstrated drug specific effects through increased activation of the anterior cingulate and decreased activation of the caudate. A direct comparison of methylphenidate and atomoxetine showed a similar recruitment in prefrontal regions but specific effects of methylphenidate in the anterior cingulate and caudate. This further supported the notion that dopaminergic processes were making a specific and dissociable contribution during response inhibition. In Chapter 3 the pharmacoimaging correlates of error awareness were examined using the EAT. This study examined the fMRI data obtained whilst testing the cohort described in Chapter 2. Methylphenidate, but not atomoxetine or citalopram, significantly improved error awareness behaviour during the EAT. Methylphenidate, versus the other drug conditions, was also associated with specific BOLD activation differences in the dorsal anterior cingulate cortex and inferior parietal lobe for errors made with versus without awareness. These findings suggested that dopaminergic, rather than noradrenergic or serotonergic, mechanisms might also be important during error awareness. Accordingly, the final experiment in this thesis sought to examine specific dopamine receptor mechanisms of executive control. In Chapter 4 the role of the D2 receptor during response inhibition and error awareness was explored. Twenty-five (25) males received acute doses of cabergoline (1.25mg) and placebo before undertaking the SST and EAT. During the SST cabergoline was able to selectively reduce stop signal reaction time without a concomitant effect on reaction time variability or overall response speed. Cabergoline was, however, unable to improve action restraint in the go no-go component of the EAT. This suggested a specific and dissociable role for the D2 receptor in the action cancellation but not action restraint, which was consistent with the findings of Chapters 1 and 2. Cabergoline was also able to enhance the conscious perception of errors during the EAT, suggesting D2 mechanisms during error awareness, which was supportive of the findings in Chapter 3. In summary, this series of experiments showed that dopaminergic, and potentially D2, mechanisms are specifically implicated in the neurobiology of human executive control. Further experiments with more specific D2 agents, combined imaging paradigms and refined task design would extend these findings.

A lack of inhibitory control has been suggested to be the core deficit in attention-deficit/hyperactivity disorder (ADHD), especially in adults. This means that a primary deficit in inhibition mediates a cascade of secondary deficits in other executive functions, such as attention. Impaired stopping has been claimed to support the inhibition hypothesis. However, executive functions such as inhibition and attention are hard to disentangle. To use event-related potentials in adult patients with ADHD to show that impaired stopping is associated with abnormalities of attention. The stop signal task was presented to 24 adults with ADHD combined subtype and 24 controls. Stop event-related potentials are distorted by overlap from event-related potentials to other stimuli in close temporal proximity, but we applied a method (Adjar level 2) to effectively remove this overlap. In line with an inhibitory control deficit, the stop signal reaction time was longer in adults with ADHD (F(1,46) = 7.12, P<.01) whereas there was no significant difference for go stimulus reaction time. Overlap-free stop event-related potentials revealed smaller stop P3s in adults with ADHD (F(1,44) = 4.20, P<.05). In children with ADHD, this has been interpreted to reflect deficient inhibitory control. However, controls were also found to have larger early responses in the auditory cortex (N1) when stop signals resulted in successful stops, relative to failed stops, signifying increased attention (F(1,23) = 11.88, P<.01). This difference was completely absent in adults with ADHD. Disturbed attentional processing of the stop signal contributed to impaired stopping in adults with ADHD. This finding may have implications for treatment.

Evidence from animal, clinical, and imaging studies suggests that the basal ganglia and their frontal connections mediate motor inhibition, but the role of dopamine remains unclear. The aim of our study was to investigate, for the first time, whether levodopa medication influences motor inhibition and conflict resolution on the conditional stop-signal reaction time task in patients with Parkinson's disease (PD) tested on or off their medication. Sixteen PD patients and 17 healthy controls performed the conditional stop-signal reaction time (SSRT) task, which requires inhibition of responses when a stop signal is presented on "critical" trials. Additionally, on "non-critical" trials, participants are instructed to ignore the stop signal and respond, thus generating conflict between motor inhibition and initiation; and conflict-induced slowing (CIS) on these "non-critical" trials. Levodopa medication did not significantly influence response initiation, inhibition (SSRT) or the measure of conflict resolution (CIS). Compared to healthy controls, PD patients showed significantly worse response initiation and inhibition both on and off their levodopa medication. Our results suggest that motor inhibition or conflict-induced slowing on the conditional stop-signal RT task are not altered by dopamine replacement in PD. This conclusion is consistent with evidence from animal studies and clinical pharmacological investigations suggesting a role for noradrenaline in motor inhibition and impulsivity.

Transcranial direct current stimulation (tDCS) is a noninvasive method of modulating human brain activity and potentially alters performance in cognitive tasks. Often it is assumed that effects of tDCS modulation depend on the polarity-anodal stimulation typically boost cognitive processes whereas cathodal stimulation hampers them. While most tDCS research focusses on the effects of anodal stimulation, cathodal tDCS effects are underexplored. In the present study, cathodal tDCS over the right dorsolateral prefrontal cortex (rDLPFC) was used to potentially hamper the response inhibition process as measured by the stop-signal task (SST). A 9 cm2 cathode was always positioned over the rDLPFC while the 35 cm2 anode was placed over the left deltoid. We contrasted a cathodal stimulation condition (that is assumed to reduce neural processing) with sham stimulation and expected a decrease in SST performance after cathodal tDCS, as evidenced by an increase in stop-signal reaction time (SSRT). In a sample of N = 45 healthy adults, a significant Time × tDCS condition interaction emerged, indicating an increase in SSRT after cathodal tDCS. In a recent study by Friehs and Frings (Journal of Experimental Psychology: Human Perception and Performance, 2018), using a similar study design and stimulation protocol, single-session anodal tDCS over the rDLPFC was used to enhance SST performance as indicated by an acceleration of SSRT. In concert, these results suggest that response inhibition is tied to the neural state of the rDLPFC.

According to the dual mechanisms of control (DMC), reactive and proactive control are involved in adjusting behaviors when maladapted to the environment. However, both contextual and inter-individual factors increase the weight of one control mechanism over the other, by influencing their cognitive costs. According to one of the DMC postulates, limited reactive control capacities should be counterbalanced by greater proactive control to ensure control efficiency. Moreover, as the flexible weighting between reactive and proactive control is key for adaptive behaviors, we expected that maladaptive behaviors, such as risk-taking, would be characterized by an absence of such counterbalance. However, to our knowledge, no studies have yet investigated this postulate. In the current study, we analyzed the performances of 176 participants on two reaction time tasks (Simon and Stop Signal tasks) and a risk-taking assessment (Balloon Analog Risk Taking, BART). The post-error slowing in the Simon task was used to reflect the spontaneous individuals’ tendency to proactively adjust behaviors after an error. The Stop Signal Reaction Time was used to assess reactive inhibition capacities and the duration of the button press in the BART was used as an index of risk-taking propensity. Results showed that poorer reactive inhibition capacities predicted greater proactive adjustments after an error. Furthermore, the higher the risk-taking propensity, the less reactive inhibition capacities predicted proactive behavioral adjustments. The reported results suggest that higher risk-taking is associated with a smaller weighting of proactive control in response to limited reactive inhibition capacities. These findings highlight the importance of considering the imbalanced weighting of reactive and proactive control in the analysis of risk-taking, and in a broader sense, maladaptive behaviors.

Effective response inhibition is crucial for daily functioning. Behavioural inhibition can be assessed using the Stop Signal Task (SST), which requires coordinated activation across a complex network of brain regions, ultimately modulating corticospinal excitability (CSE). Importantly, CSE is not only modulated by excitatory drive but also by intracortical inhibitory processes such as short intracortical inhibition (SICI), which reflects the inhibitory activity of the GABAA receptors within the primary motor cortex. This review examines a series of studies exploring CSE changes, measured through Transcranial Magnetic Stimulation (TMS) applied online, i.e., during SST performance. We mainly focused on the temporal dynamics of CSE and SICI during the SST across healthy and clinical populations, highlighting differences between task-related and unrelated muscles, examining both global and selective modulations in proactive and reactive versions of the SST. Our discussion addresses the methodological and theoretical considerations involved in recording CSE online and questions the SST's effectiveness in accurately capturing inhibitory processes. Additionally, we analyse findings from motor-related disorders in clinical populations to identify specific abnormalities in CSE modulation and their underlying neural mechanisms. By summarizing the existing literature, we aim to offer a comprehensive view of the temporal dynamics of CSE, identifying key factors and methodologies that influence CSE modulation. This review seeks to prompt future directions in cognitive neuroscience research and potential clinical applications.