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The maturation of task set-related activation supports late developmental improvements in inhibitory control.

ABSTRACT: The ability to voluntarily inhibit a single response is evident early in development, even as the ability to maintain an inhibitory "task set" continues to improve. To date, functional neuroimaging studies have detailed developmental changes in systems supporting inhibitory control exerted at the single-trial level, but changes underlying the ability to maintain an inhibitory task set remain little understood. Here we present findings from a functional magnetic resonance imaging study that characterizes the development of systems supporting both transient (trial-related) and sustained (task set-related) activation during performance of the antisaccade task-an oculomotor test of inhibitory control (Hallett, 1978). Transient activation decreased from childhood to adolescence in regions known to support inhibitory processes and oculomotor control, likely reflecting less effortful response production. In contrast, sustained activation increased to adulthood in regions implicated in control. Our results suggest that development of the ability to maintain a task set is primary to the maturation of inhibitory control and, furthermore, that this ability is still immature in adolescence.

SUBMITTER: Velanova K

PROVIDER: S-EPMC2788337 | biostudies-other | 2009 Oct

REPOSITORIES: biostudies-other

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The maturation of task set-related activation supports late developmental improvements in inhibitory control.

Velanova Katerina K Wheeler Mark E ME Luna Beatriz B

The Journal of neuroscience : the official journal of the Society for Neuroscience 20091001 40

The ability to voluntarily inhibit a single response is evident early in development, even as the ability to maintain an inhibitory "task set" continues to improve. To date, functional neuroimaging studies have detailed developmental changes in systems supporting inhibitory control exerted at the single-trial level, but changes underlying the ability to maintain an inhibitory task set remain little understood. Here we present findings from a functional magnetic resonance imaging study that chara ...[more]

PMID: 19812330

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Project description:Healthy, older adults are widely reported to experience cognitive decline, including impairments in inhibitory control. However, this general proposition has recently come under scrutiny because ageing effects are highly variable between individuals, are task dependent, and are sometimes not distinguished from general age-related slowing. We recently developed the minimally delayed oculomotor response (MDOR) task in which participants are presented with a simple visual target step, and instructed to saccade not to the target when it appears (a prosaccade response), but when it disappears (i.e. on target offset). Varying the target display duration (TDD) prevents offset timing being predictable from the time of target onset, and saccades prior to the offset are counted as errors. A comparison of MDOR task performance in a group of 22 older adults (mean age 62 years, range 50-72 years) with that in a group of 39 younger adults (22 years, range 19-27 years) demonstrated that MDOR latency was significantly increased in the older group by 34-68 ms depending on TDD. However, when MDOR latencies were corrected by subtracting the latency observed in a standard prosaccade task, the latency difference between groups was abolished. There was a larger latency modulation with TDD in the older group which was observed even when their generally longer latencies were taken into account. Error rates were significantly increased in the older group. An analysis of the timing distribution of errors demonstrated that most errors were failures to inhibit responses to target onsets. When error distributions were used to isolate clear inhibition failures from other types of error, the older group still exhibited significantly higher error rates as well as a higher residual error rate. Although MDOR latency in older participants may largely reflect a general slowing in the oculomotor system with age, both the latency modulation and error rate results are consistent with an age-related inhibitory control deficit. How this relates to performance on other inhibitory control tasks remains to be investigated.

Project description:Deficits characteristic of attention deficit/hyperactivity disorder (ADHD), including poor attention and inhibitory control, are at least partially alleviated by factors that increase engagement of attention, suggesting a hypodopaminergic reward deficit. Lapses of attention are associated with attenuated deactivation of the default mode network (DMN), a distributed brain system normally deactivated during tasks requiring attention to the external world. Task-related DMN deactivation has been shown to be attenuated in ADHD relative to controls. We hypothesised that motivational incentives to balance speed against restraint would increase task engagement during an inhibitory control task, enhancing DMN deactivation in ADHD. We also hypothesised that methylphenidate, an indirect dopamine agonist, would tend to normalise abnormal patterns of DMN deactivation.We obtained functional magnetic resonance images from 18 methylphenidate-responsive children with ADHD (DSM-IV combined subtype) and 18 pairwise-matched typically developing children aged 9-15 years while they performed a paced Go/No-go task. We manipulated motivational incentive to balance response speed against inhibitory control, and tested children with ADHD both on and off methylphenidate.When children with ADHD were off-methylphenidate and task incentive was low, event-related DMN deactivation was significantly attenuated compared to controls, but the two groups did not differ under high motivational incentives. The modulation of DMN deactivation by incentive in the children with ADHD, off-methylphenidate, was statistically significant, and significantly greater than in typically developing children. When children with ADHD were on-methylphenidate, motivational modulation of event-related DMN deactivation was abolished, and no attenuation relative to their typically developing peers was apparent in either motivational condition.During an inhibitory control task, children with ADHD exhibit a raised motivational threshold at which task-relevant stimuli become sufficiently salient to deactivate the DMN. Treatment with methylphenidate normalises this threshold, rendering their pattern of task-related DMN deactivation indistinguishable from that of typically developing children.

Project description:BACKGROUND:Altered 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. METHODS:We 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. RESULTS:Only 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. CONCLUSIONS:Stimuli 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.

Project description:Considerable effort has been made to measure and understand the effects of ageing on inhibitory control using a range of behavioural tasks. In the minimally delayed oculomotor response (MDOR) task, participants are presented with a simple visual target step with variable target display duration (TDD), and instructed to saccade to the target not when it appears (a prosaccade response), but when it disappears (i.e., on target offset). Using this task, we recently found higher error rates and longer latencies for correct responses in older compared to younger participants. Here we have used a modified MDOR task, in which participants were presented with static placeholders identifying potential target positions (increasing spatial information), and three TDDs rather than two (reducing temporal predictability). We found that the yield of analysable trials was generally higher with this modified task and in 28 older (mean ± SD age: 65 ± 7 y) and 25 younger (26 ± 7 y) participants the total overall error rate was again higher in the older group (30 ± 18% vs. 16 ± 11%). An analysis of the temporal distribution of responses demonstrated a pronounced peak in error production around 150 ms (young) or 200 ms (old) after target onset. When we recalculated the error rate focusing on these errors, it was again significantly higher in the older group. The latency of correct responses (to offsets) was significantly increased in the older group, although much of this increase was accounted for by expected age-related visuomotor slowing. However, both latency and distribution data suggested that while older participants could generate increased levels of inhibition, they could not maintain these levels as efficiently as the younger participants. In 24 participants (15 old, 9 young) who completed both versions of the MDOR task, neither latency nor error rates differed significantly between versions. These results confirm an inhibitory control deficit in healthy older participants, and suggest that the dynamics of inhibitory control are also affected by ageing. The modified MDOR task yields more data while not altering basic performance parameters.

Dataset Information

The maturation of task set-related activation supports late developmental improvements in inhibitory control.

Publications

The maturation of task set-related activation supports late developmental improvements in inhibitory control.

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