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what developmental biological changes lead to improvement in inhibitory control and working memory

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  • Journal List
  • Dev Cogn Neurosci
  • 5.1(iv); 2011 Oct
  • PMC3181104

Dev Cogn Neurosci. 2011 Oct; one(4): 517–529.

Developmental changes in brain function underlying the influence of advantage processing on inhibitory control

Aarthi Padmanabhan,a, b, c, * Charles F. Geier,a, b, c Sarah J. Ordaz,a, b Theresa Teslovich,d and Beatriz Lunaa, b, c

Aarthi Padmanabhan

aDepartment of Psychiatry, University of Pittsburgh, Pittsburgh, PA, USA

bDepartment of Psychology, University of Pittsburgh, Pittsburgh, PA, USA

cCenter for the Neural Basis of Cognition, Pittsburgh, PA, USA

Charles F. Geier

aSection of Psychiatry, Academy of Pittsburgh, Pittsburgh, PA, Us

bDepartment of Psychology, University of Pittsburgh, Pittsburgh, PA, United states

cHeart for the Neural Basis of Cognition, Pittsburgh, PA, Usa

Sarah J. Ordaz

aDepartment of Psychiatry, University of Pittsburgh, Pittsburgh, PA, U.s.a.

bDepartment of Psychology, University of Pittsburgh, Pittsburgh, PA, U.s.

Theresa Teslovich

dDepartment of Psychiatry, Weill Medical College of Cornell University, New York, NY, USA

Beatriz Luna

aDepartment of Psychiatry, Academy of Pittsburgh, Pittsburgh, PA, United states

bSection of Psychology, University of Pittsburgh, Pittsburgh, PA, U.s.

cMiddle for the Neural Basis of Cognition, Pittsburgh, PA, Us

Received 2011 Feb 4; Revised 2011 Apr eleven; Accepted 2011 Jun ten.

Abstract

Adolescence is a period marked by changes in motivational and cognitive brain systems. However, the development of the interactions betwixt reward and cerebral control processing are but commencement to be understood. Using consequence-related functional neuroimaging and an incentive modulated antisaccade chore, we compared blood-oxygen level dependent activity underlying motivated response inhibition in children, adolescents, and adults. Behaviorally, children and adolescents performed significantly worse than adults during neutral trials. Yet, children and adolescents showed meaning performance increases during advantage trials. Adults showed no performance changes across conditions. fMRI results demonstrated that all groups recruited a similar circuitry to support task performance, including regions typically associated with rewards (striatum and orbital frontal cortex), and regions known to be involved in inhibitory control (putative frontal and supplementary middle fields, and posterior parietal cortex, and prefrontal loci). During rewarded trials adolescents showed increased activity in striatal regions, while adults demonstrated heightened activation in the OFC relative to children and adolescents. Children showed greater reliance on prefrontal executive regions that may exist related to increased endeavour in inhibiting responses. Overall, these results indicate that response inhibition is enhanced with reward contingencies over development. Adolescents' heightened response in striatal regions may be one factor contributing to reward-biased conclusion making and perhaps risk taking behavior.

Keywords: Adolescence, Reward, Inhibitory control, Antisaccade, fMRI

one. Introduction

Adolescence is a unique menstruation of evolution characterized by immature reward processing and inconsistencies in inhibitory command, an important, fundamental component of the cognitive command of behavior. Adolescent behavior is distinct from childhood and adulthood, as evidenced by heightened incidents of sub-optimal or young decision-making. Although adolescents have improved conclusion making skills compared to children, unique immaturities exist that often result in a peak in risk taking behavior. We define adulthood as the model system and describe functions and behavior by younger individuals that deviate from this system every bit "immature" (for review encounter Luna et al., 2010). While of import work has been done to delineate adolescent immaturities underlying advantage processing (Bjork et al., 2004, Cohen et al., 2010, Ernst et al., 2005, Ernst et al., 2006, Eshel et al., 2007, Galvan, 2010, May et al., 2004, van Leijenhorst et al., 2009), and cerebral control (Bunge et al., 2002, Levin et al., 1991, Liston et al., 2006, Luna et al., 2004, Paus et al., 1990, Ridderinkhof et al., 1999, Ridderinkhof and van der Molen, 1997, Williams et al., 1999; for review run across Luna, 2009), the influence of incentives on components of cerebral control within a developmental context is relatively understudied (for review run across Geier and Luna, 2009). Furthermore, in order to improve understand immature processes that are unique to the boyish period, boyish processes must be contrasted with the preceding stage of childhood and the post-obit mature stage of adulthood.

Behavioral bear witness conspicuously indicates that adolescents can demonstrate mature levels of inhibitory control, simply do and so inconsistently compared to adults (Bedard et al., 2002, Luna et al., 2004, Ridderinkhof et al., 1999, Van den Wildenberg and van der Molen, 2004, Velanova et al., 2009, Wise et al., 1975). Furthermore, neuroimaging studies have demonstrated that adolescents performing tasks of inhibitory control exhibit a singled-out neurofunctional contour, likely reflecting connected brain immaturities (Luna et al., 2001, Rubia et al., 2007, Velanova et al., 2008, Velanova et al., 2009). During adolescence, fundamental reward processing and control regions including the striatum and prefrontal cortex demonstrate continued gray thing thinning (Giedd et al., 1996, Gogtay et al., 2004, Sowell et al., 1999, Toga et al., 2006). Similarly, white matter connections between these regions strengthen, indicating increased fidelity/speed of distal neuronal transmission, which may support the functional integration necessary for complex behavior (Asato et al., 2010). The transition to mature behavior coupled with however-young neural office may be reflected in these maturational processes and in functional neuroimaging studies that have demonstrated that in the absence of performance differences, adolescents demonstrate differences in recruitment of key encephalon regions. For example, adolescents who demonstrate adult-levels of mature behavior (i.e. no performance differences in laboratory tasks of knowledge), demonstrate increased activity of prefrontal cortex, suggesting increased effort required to perform the task at equivalent levels (Luna et al., 2001; for review meet Luna, 2009).

One particularly robust and reliable analysis of developmental changes in inhibitory control behavior and the neural systems that support information technology is the antisaccade (AS) chore (Hallett, 1978). The Equally job, which requires a participant to inhibit the reflexive tendency to await toward a sudden presentation of a peripheral stimulus and instead make an eye movement (saccade) to its mirror location, has extensively been used to characterize the neural ground of inhibitory control in both humans and non-human being primates (Brown et al., 2007, Butler et al., 1999, Cherkasova et al., 2002, Everling and Fischer, 1998, Fischer and Weber, 1996, Matsuda et al., 2004, Munoz et al., 1998, Munoz and Everling, 2004, Schlag-Rey et al., 1997). Work in humans and non-homo primates have delineated a widely distributed circuitry that supports AS performance including the frontal, supplementary, and parietal eye fields (FEF, SEF, PEF respectively), as well every bit prefrontal cortex (PFC) and various subcortical structures such as striatum, thalamus, and cerebellum (Brown et al., 2006, Luna and Sweeney, 1999, Matsuda et al., 2004). Neuroimaging studies suggest that encephalon role underlying AS performance continues to demonstrate immaturities (Luna et al., 2001, Velanova et al., 2008, Velanova et al., 2009), despite behavioral bear witness suggesting that the rate of inhibitory AS errors begins to reach developed levels in mid adolescence (Fischer et al., 1997, Klein and Foerster, 2001, Luna et al., 2004, Munoz et al., 1998). These functional immaturities include the recruitment of brain processes that back up Every bit fault processing (Velanova et al., 2008), and the ability to retain an inhibitory response state (Velanova et al., 2009), which proceed to improve into immature adulthood.

Immaturities in reward processing are also axiomatic during adolescence. Converging lines of prove from single-cell recording, lesion and neuroimaging studies take delineated a circuitry related to reward processing that originates in the ventral tegmental expanse of the midbrain, extending through the ventral striatum (VS) (including the nucleus accumbens), and projecting out to medial and ventral regions of the PFC (including the orbital frontal cortex (OFC)), and the anterior cingulate cortex (ACC) (Apicella et al., 1991, Bjork et al., 2004, Breiter et al., 2001, Chambers et al., 2003, Delgado et al., 2000, Delgado et al., 2003, Elliott et al., 2003, Hikosaka and Watanabe, 2000, Knutson et al., 2000, Roesch and Olson, 2003, Roesch and Olson, 2004, Schultz et al., 2000, Thut et al., 1997, van Leijenhorst et al., 2009, Wise, 2002). Developmental fMRI studies on reward processing have found age related differences in the magnitude of recruitment of striatal and prefrontal regions (Bjork et al., 2004, Ernst et al., 2005, Galvan et al., 2006, Guyer et al., 2006, May et al., 2004, van Leijenhorst et al., 2009). In some studies, adolescents were found to exhibit a relative decrease of VS, OFC and mesial PFC recruitment during advantage cue and anticipation (Bjork et al., 2004, Bjork et al., 2007, Bjork et al., 2010). In contrast, other work has suggested that adolescents demonstrate increased activity of VS primarily during reward receipt (Ernst et al., 2005, Galvan et al., 2006, van Leijenhorst et al., 2009, van Leijenhorst et al., 2010). Our previous work has provided prove indicating that adolescents demonstrate an initial decrease in recruitment of the VS during incentive cue cess simply markedly increased VS activity during reward apprehension relative to adults (Geier et al., 2010). Although these results indicate that immaturities are present during adolescence in reward processing, it remains to be seen whether such immaturities are also present in childhood. Moreover, studies that have considered childhood to adulthood have focused on reward reactivity exclusively but non on its furnishings on cognitive control (Cohen et al., 2010, Galvan et al., 2006, van Leijenhorst et al., 2009), Recently, van Leijenhorst et al. (2010) using a gambling chore designed to assess the neural correlates of high-take chances and low-risk monetary gambles, demonstrated that reward related activeness peaked in adolescence compared to children and adults whereas cognitive control related activity followed a linear trajectory. This finding suggests that an over-reactive advantage system coupled with a still developing cognitive system may account for unique influences of rewards on determination making.

In the present study, nosotros aimed at studying the effects of cerebral control on reward processing in childhood, adolescence and adulthood. We hypothesized that adolescents would show enhanced activity in key advantage related regions relative to adults (Cohen et al., 2010, Galvan et al., 2006, van Leijenhorst et al., 2009, van Leijenhorst et al., 2010), Moreover, we expected a similarly singled-out boyish response when compared to children. Given our prior finding that rewards improve Equally performance (Geier et al., 2010) and raise activity in oculomotor control regions, nosotros hypothesized that improved As performance would be accompanied by increased recruitment of oculomotor command regions known to support antisaccade processing (Luna et al., 2001, Luna et al., 2004). Finally, we predicted that children would demonstrate increased recruitment of prefrontal cognitive command regions (such every bit the anterior cingulate cortex and dorsolateral prefrontal cortex) in line with previous work demonstrating immature over-reliance on prefrontal systems in children when performing cerebral tasks (Luna et al., 2001).

2. Materials and methods

2.i. Participants

Nosotros recruited 34 participants for this report. Four children were excluded due to non-compliance with the task instructions. We thus report on thirty healthy, correct-handed participants, ten adults (ages 18–25, mean = twenty.6 (±two.two st dev); six females), 10 adolescents (ages 14–17; mean = xv.eight (±1.2 st dev), six females), and ten children (ages 8–13 years, mean = 11.ane (±1.5 st dev), six females). Historic period groups were defined based on previous behavioral studies indicating differential cognitive performance on the AS chore (Luna et al., 2004). Participants were native English speakers with no personal or first-degree relative history of neurological illness, brain injury, or psychiatric illness every bit determined past interview. Vision was normal or corrected to normal using MRI uniform glasses or contact lenses. Full scale IQ scores determined using the WASI (Wechsler Abbreviated Scale of Intelligence) were in a higher place 85 and there were no meaning differences in IQ across historic period groups (Children: mean = 112.4 (±13.viii st. dev), Adolescents: mean = 108.6 (±vii.5 st. dev), Adults: 116.7 (±10.2 st. dev), p = .263). Immediately prior to scanning, participants were given explicit verbal instructions and trained on the antisaccade (AS) and visually guided saccades (VGS) tasks in a separate behavioral testing room till they became comfortable performing the chore (corresponded to 4–five trials each on average). Participants as well spent approximately fifteen min in a mock scanner to acclimate them to the MR environment (Rosenberg et al., 1997). Experimental procedures for this written report complied with the Code of Ethics of the World Medical Association (1964 Declaration of Helsinki) and the Institutional Review Board at the University of Pittsburgh. Participants were paid for their participation in the study with a chance to win extra coin during the fMRI task.

2.2. Behavioral epitome

At the onset of each AS trial, participants were first presented with one of ii incentive cues (1500 ms) (Fig. 1). For rewarded trials, the cue consisted of iii rectangles containing dollar signs ($ $ $), indicating that money could exist earned on that trial if correctly performed. Participants were told that they could win up to Usa $25 based on their performance during the task. Yet, they did not know how much they could win on any given trial in order to prevent them from keeping a running tally of their earnings and invoking processes (i.east. working memory) separate from inhibitory command and reward processing. For neutral trials, the three sequent rectangles each independent a dash (– – –), which indicated that no monetary gain was at stake for that trial. After the initial cue, a cardinal red fixation cantankerous subtending ∼0.vii° of visual angle appeared (3000 ms), instructing participants to set for the target stimulus. The red central fixation then disappeared and a horizontally peripheral target stimulus (yellow spot, subtending ∼0.5°) appeared (1500 ms) at an unpredictable location on the horizontal meridian (±3°, 6°, or 9°). Participants were instructed to refrain from looking at the stimulus when it appeared but instead move their eyes to its mirror location. Target location was randomized within each run. During the VGS trials, participants were presented with a greenish fixation cross (1500 ms) which instructed them to wait toward the peripheral stimulus when it appeared. No incentive cue was provided for VGS trials. The VGS trials were randomly interspersed between the Equally trials to minimize the possibility that participants would constitute an inhibitory response set (Velanova et al., 2009), but were not further analyzed. As indicated in previous studies, (Ollinger et al., 2001b, Ollinger et al., 2001a), the inter-trial fixation period was jittered between intervals of 1.5, 3, or 4.5 s (uniformly distributed) and consisted of participants simply fixating a fundamental white cross on a black background. Participants performed 3 functional runs of the job (v min ii s each in elapsing) for a total of 30 reward As trials, xxx neutral AS trials and 15 VGS trials.

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Rewarded antisaccade task schematic. A row of three dollar signs indicated that participant could win money contingent on their performance in the upcoming trial (reward trial). A row of 3 horizontal dashed lines indicated that no coin could be won in the upcoming trial (neutral trial). Incentive cues were presented for one.5 s. Post-obit that, a red fixation cross appeared for 3 s. A peripheral calorie-free appeared for 1.five s during which, participants were instructed to generate a saccade to its mirror location.

2.3. Middle tracking

Middle movement measurements were obtained in the MR environment using a long-range optics middle-tracking system (Model R-LRO6, Applied Science Laboratories, Bedford, MA). Simultaneous video monitoring was also used to clinch task compliance. 9-point calibrations were performed at the beginning of the session and between runs as necessary. Stimuli were presented using E-Prime (Psychology Software Tools, Inc., Pittsburgh, PA), projected onto a flat screen positioned behind the magnet. Participants viewed the screen using a mirror mounted on the RF head curlicue. Center-movement information were analyzed and scored offline using ILAB (Gitelman, 2002) in conjunction with an in-house scoring suite. Variables of interest included latencies for correct AS trials and error charge per unit (the number of inhibitory failures/total number of scorable trials) during rewarded and neutral trials. A correct response in the AS chore was one in which the starting time heart movement during the saccade response epoch with velocity greater than or equal to 30°/s (Gitelman, 2002) was made toward the mirror location of the peripheral cue, and extended beyond a 2.five°/visual bending primal fixation zone. AS errors (also often referred to every bit prosaccades) occurred when the first saccade during the saccade response epoch was directed toward the suddenly appearing peripheral stimulus and exceeded the ii.v°/visual angle central fixation zone. Participants commonly corrected inhibitory errors indicating that they understood the educational activity but were unable to terminate the initial reflexive gaze to the visual stimulus.

two.4. fMRI

2.4.1. Epitome acquisition and preprocessing

Imaging data were acquired using a Siemens 3-Tesla MAGNETOM Allegra (Erlangen, Germany) organisation with a standard radiofrequency (RF) head coil at the Brain Imaging Research Middle, Academy of Pittsburgh, Pittsburgh, PA. Structural images were acquired using a sagittal magnetization prepared rapid gradient repeat (MPRAGE) T1-weighted pulse sequence with 224 slices with 0.7825 mm piece thickness. Functional images were caused using a gradient echo echo-planar (EPI) sequence sensitive to claret-oxygen-dependent (Bold) contrast (T2*) (TR = 1.v s, TE = 25 ms, flip bending = 70°, voxel size = 3.125 × 3.125 × iv mm in-airplane resolution, 216 volumes). Twenty-nine slices per volume were nerveless with no gap and aligned to the anterior and posterior commissure (AC–PC) airplane. The first four volumes in each run were discarded to allow stabilization of longitudinal magnetization.

Imaging data were preprocessed using FSL (FMRIB Software Library; Smith et al., 2004). Briefly, our preprocessing procedures included the following: Start, slice-timing correction was performed, adjusting for interleaved slice acquisition. Images were rigid-torso move corrected past aligning all volumes with the volume acquired in the eye of the fMRI session. Rotational and translational caput motion estimates were calculated. Post-obit encephalon extraction (using FSL'southward brain extraction tool, BET) (Smith, 2002), functional images were affine registered and warped to structural MPRAGE images in Talairach space (Talairach and Tournoux, 1988), using both the FLIRT and FNIRT tools in FSL (Jenkinson and Smith, 2001). No participants were excluded due to motility, instead the temporal derivative of the relative deportation from the eye volume for each run was calculated for each volume in the x, y and z directions. Magnitude of the velocity was then calculated past taking the square root of the sum of squares of the ten, y and z components for each volume. Volumes with a velocity (in mm per TR) of over ane.2 mm were removed (censored) from subsequent analyses. Participant groups did not differ in number of volumes removed due to excessive motion (censored three volumes from two children and one volume from 2 adolescents). Images were so spatially smoothed with a v mm full-width at one-half maximum (FWHM) Gaussian smoothing kernel and high-laissez passer filtered (sigma = 30 due south) to remove low frequency drift. Information from each run were and then scaled to a mean of one hundred and multiple runs were concatenated.

2.4.ii. Data analyses

AFNI (Analysis and Visualization of Functional Neuroimages) software (Cox, 1996) was used for individual subject deconvolution as well as subsequent group analyses. Deconvolution methods followed steps delineated previously (Ward, 1998). Briefly, our model consisted of 2 orthogonal regressors of interest for reward and neutral right AS trials, as well every bit regressors for incorrect AS trials and all VGS trials. Linear and non-linear trends and vi motion parameters were also included as nuisance regressors. A unique estimated impulse response function (i.eastward. hemodynamic response function) for each regressor of interest (right reward and neutral AS trials) was adamant past a weighted linear sum of eight sine basis functions multiplied by information determined least squares estimated beta weights. The estimated impulse response function reflects the estimated Bold response to a blazon of trial (reward Equally trial) after controlling for variations in the BOLD betoken due to other regressors. We fabricated no assumptions near the shape of the function. We specified the duration of the estimated response from the trial onset (0 s) to 24 southward (17 TRs) post trial onset, a sufficient time window for the hemodynamic response to peak and return to baseline, which was defined as the jittered fixation periods betwixt trials.

For grouping analyses, impulse response function values associated with correct reward and neutral AS trials from each participant were entered into a voxel-wise linear mixed furnishings model, with 'subjects' as a random factor and fourth dimension (0–16 TRs) and 'incentive' (reward, neutral) as within-group factors, and 'age-grouping' (children, adolescent, developed) every bit between-grouping stock-still factors. The 'main upshot of fourth dimension' image that resulted from this model was used every bit a base image from which functional regions of involvement (ROIs), were defined (run into below) because it shows all regions that demonstrate a significant modulation from baseline across all groups and conditions, making it unbiased with respect to all effects of interest and has been reliable in delineating the basic circuitry recruited in our report (Geier et al., 2010, Velanova et al., 2008).

Functionally defined regions of interest were determined using methods already established in the literature (Wheeler et al., 2005). First, the main effect of time map was corrected for multiple comparisons using a combination of cluster size and individual voxel probabilities and parameters adamant following a Monte Carlo simulation using AFNI's AlphaSim program. This assay specified that 23 contiguous voxels along with a single-voxel threshold of p < 0.001 was required to achieve a corrected, cluster-level alpha value of 0.05.

Second, peak voxels in the corrected main event of time map were identified using an automatic search algorithm. Twelve-millimeter diameter spheres were centered on these tiptop voxels, resulting in a 'sphere map'. Finally, a conjunction of the 'sphere map' and the corrected main effect of time map yielded a functional ROI map, which was used as a mask for subsequent analyses in social club to excerpt time course values for each participant. Due to the relatively small size of the VS, a ten millimeter diameter sphere (encompassing approximately 20 voxels) was manually traced around peak voxels that fell within the region (equally defined by the Talairach and Tourneaux atlas (Talairach and Tournoux, 1988)) in both hemispheres.

We focused our subsequent analyses on these functionally defined clusters that fell within the boundaries of several a priori anatomical regions of interest purportedly involved in oculomotor command and reward processing. These included the paracentral sulcus, which is considered to correspond the SEF, the superior aspect of the precentral sulcus, which is considered to represent the FEF (Curtis and Connolly, 2008, Luna et al., 1998), and the SPL, which is considered to exist the parietal eye field (Curtis and Connolly, 2008, Luna et al., 1998), the dorsal and ventral striatum, the ACC, and the OFC.

Mean estimated time courses from each participant were extracted from the voxels constituting each corrected sphere mask across both reward and neutral incentives. Mean time course values at each time betoken (0–16 TRs) were entered into a repeated measures ANOVA using age grouping as the betwixt subjects gene and time and incentive type as within subjects factors. Below, we report regions that demonstrated an age-group by time, incentive-condition by time and/or an age-group by incentive-condition by fourth dimension interaction across the modeled window of 17 TRs. While it is crucial that furnishings be determined based on the entire modeled timecourse, extended timecourses can often incur noise, especially at the tail-end of the window, which can undermine the power to assess magnitude differences. Therefore, we also analyzed regions across the first half of the modeled response (8 TRs), which encompassed the rise and peak of the hemodynamic response.

3. Results

three.1. Beliefs

Behavioral results showed a main effect of incentive type for AS error charge per unit, (F(1,27) = viii.357, p < 0.01) with more than errors occurring in the neutral vs. advantage weather. There was a trend for a main effect of age grouping on rate of Every bit errors (p = .094). Simple effects of age group during the neutral trials were evident with children (t(eighteen) = 3.287, p < .005) and adolescents (t(18) = 2.172, p < .05) demonstrating worse operation during neutral trials relative to adults. In that location were no differences between children and adolescents during neutral trials (p = 0.242).

There was an incentive type past age group interaction (F(2,27) = four.884, p < .05). There was no effect of age group during rewarded trials. Within each age group, children (t(9) = −4.71, p < .001) and adolescents (t(nine) = −2.24, p < .05), only not adults (p = .46), generated fewer errors during rewarded trials compared to neutral. Postal service-hoc comparisons indicated that all three groups demonstrated equivalent functioning on reward trials (Fig. 2a). There were no differences in the number of dropped trials (i.due east. participant did not try to perform the task) between rewarded and neutral conditions across historic period groups.

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Behavioral results. (A) Antisaccade error rate (% errors) for children (left), adolescents (middle) and adults (correct) for both rewarded (greyness bars) and neutral (blackness bars) trials. (B) Latencies (ms) of correct antisaccades for children (left), adolescents (middle) and adults (right) for both rewarded (gray bars) and neutral (blackness bars) trials. Single asterisk (*) indicates significance at the 0.05 blastoff level. Double asterisks (**) indicate significance at the .001 alpha level.

The latency of correct antisaccades showed a principal result of incentive blazon (F(one,27) = 209.618, p < .0001) but no main upshot of historic period group (p = .138) or age group by incentive type interaction (p = .975). All iii age-groups generated significantly faster correct anti-saccade responses during reward trials compared to neutral (children: t(9) = 2.26, p < .0001, adolescents: t(9) = 2.26, p < .0001, adults: t(9) = 2.26, p < .0001) (Fig. 2b).

three.2. Imaging

Tabular array 1 provides a summary of all regions of interest that demonstrated a main effect of time. Main effect of time effects across conditions and age groups demonstrated robust recruitment of a distributed circuitry including frontal, supplementary, posterior parietal cortex, basal ganglia, PFC, VS and OFC (Fig. 3). Within these regions, bilateral FEF, and superior parietal cortex, did not demonstrate whatever age or incentive interactions with time (Fig. 4).

Table ane

Regions of interest demonstrating a main event of time.

Region (Broadmann area) Coordinatea
Peak F n voxels Upshot F outcome Grouping resultb F group issue
x y z
Left Frontal Eye Field (6) −22 −8 48 86.84 33 Fourth dimension 87.171 None north/a
Right Frontal Heart Field (half-dozen) 29 −11 46 82.77 33 Fourth dimension 83.314 None n/a
Left Superior Parietal Lobule (7) −25 −59 43 75.46 33 Time 83.003 None n/a
Right Superior Parietal Lobule (vii) 26 −62 43 81.96 33 Time 80.311 None north/a
Right Junior Parietal Sulcus (40) 41 −44 40 24.78 33 Age × Incentive × Time 2.730** TR > TN 4.894***
Supplementary Middle Field (6) 2 −2 52 61.seventy 33 Age × Time one.940* CN > (TN = AN) 2.232**
Right Dorsal Anterior Cingulate (24) 8 seven 34 63.53 33 Age × Time 2.484* C > (T = A) 2.484*
Left Putamen −22 four i 51.76 33 Incentive × Fourth dimension 2.857* TR > TN five.008***
Right Putamen 20 7 iv 54.21 33 Incentive × Fourth dimension 2.589* TR > TN 3.735*
Left VS −10 8 −four ix.12 19 Incentive × Time ii.343* TR > TN 4.805***
Right VS 14 8 −four 19.91 nineteen Incentive × Time 2.501* TR > TN 3.735*
OFC (47) 35 28 −11 9.83 28 Age × Incentive × Time 2.935* AR > AN ii.283**
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Activation maps for main issue of time collapsed across incentive weather and historic period groups. Threshold set at p < 0.001 (corrected). Right side of image = right encephalon.

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Fourth dimension courses showing key oculomotor control regions that showed no group differences. Meet materials and methods for how time courses were extracted. Error bars correspond ±1 standard error of the mean at each fourth dimension bespeak. For visualization purposes only, filled black circles indicating location of the masks are schematically shown above slices of the AFNI Talairach atlas, fatigued using AFNI. The circles do non reflect the actual shape of the mask. R = Right side. L = Left Side.

Across the entire modeled response (17 TRs), in right lateral OFC, in that location was a significant age-grouping by incentive by fourth dimension interaction (F(eight,108) = two.935, p < .05). Still this was due to a late increased tiptop in adults during rewarded relative to neutral trials (F(16,144) = two.283, p < .005) (Fig. v).

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Time courses separated by age group in left lateral OFC. Run into materials and methods for how time courses were extracted. Error confined represent ±1 standard error of the hateful at each time point. For visualization purposes only, filled black circles indicating location of the masks are schematically shown in a higher place slices of the AFNI Talairach atlas, drawn using AFNI. The circles practise not reflect the actual shape of the mask.

Pregnant group differences across the first half of the modeled response (viii TRs) were noted in the SEF and dorsal ACC. In SEF, there was a significant age-group by time interaction (F(14,189) = 1.940, p < .05). Post-hoc tests indicated that children demonstrated increased activeness relative to adults and adolescents during neutral (fourth dimension by age: F(xiv,189) = two.232, p < .01) only not rewarded trials (p = .11) (Fig. half-dozena). In the dorsal ACC, children demonstrated increased activity during both rewarded and neutral trials relative to adults (age by time: F(7,126) = 2.484, p < .05) (Fig. half-dozenb).

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Fourth dimension courses separated by incentive condition of regions where children demonstrated increased activeness relative to other two groups. See materials and methods for how time courses were extracted. Error bars represent ±1 standard error of the mean at each time signal. Vertical dotted lines represent the offset half of the modeled response (8 TRs) that showed a significant interaction event. For visualization purposes only, filled black circles indicating location of the masks are schematically shown above slices of the AFNI Talairach atlas, fatigued using AFNI. The circles practice not reflect the actual shape of the mask.

Across a range of regions including IPS, putamen, and VS, just adolescents demonstrated greater activity for rewarded relative to neutral trials. A significant age-grouping by incentive by time effect was found in right IPS (F(fourteen,189) = 2.730, p < .001). Post-hoc comparisons indicated that only adolescents (incentive by fourth dimension: F(seven,63) = four.894, p < .0001) demonstrated a meaning condition past time interaction, increasing activity in response to reward trials relative to neutral (Fig. 7a).

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Time courses separated past age group of regions where adolescents demonstrated a modulation past incentive condition. Run across materials and methods for how fourth dimension courses were extracted. Error bars represent ±1 standard mistake of the hateful at each time point. Vertical dotted lines represent the first half of the modeled response (8 TRs) that showed a meaning interaction effect. For visualization purposes merely, filled black circles indicating location of the masks are schematically shown above slices of the AFNI Talairach atlas template brain, drawn using AFNI. The circles do non reverberate the actual shape of the mask. R = Right hemisphere of the brain. L = Left hemisphere of the brain.

In the right putamen, a meaning incentive past time interaction was observed (F(7,189) = 2.589, p < .05). Adolescents demonstrated increased action to rewarded relative to neutral trials (incentive past time: F(seven,63) = 3.735, p < .005) whereas adults and children did not. The left putamen showed a similar blueprint of activity, with a significant incentive by time interaction (F(7,189) = 2.857, p < .05), with only adolescents showing increased activeness for rewarded relative to neutral trials (incentive by time: F = (7,63) = 5.008, p < .0001) (Fig. 7b and c).

In right ventral striatum, there was a pregnant incentive by time interaction (F(7,189) = 2.501, p < .05) and a trend for a age-group by incentive by time interaction (p = .08). Adolescents demonstrated significantly increased activity for rewarded trials relative to neutral (incentive by time F(7,63) = three.735, p < .005), only children and adults did not. In left ventral striatum, similar to the contra-lateral region, a meaning incentive by time interaction was observed (F(vii,189) = ii.343, p < .05). As before, adolescents increased activeness during rewarded trials relative to neutral (incentive by time: F(7,63) = 4.805, p < .0001) whereas adults and children did non (Fig. 7d and due east).

four. Discussion

The purpose of this study was to improve sympathize processes underlying the influence of rewards on inhibitory control in adolescence by including child and adult groups. Behavioral results indicated that rewards enhanced task performance (i.eastward. reduced latencies and mistake rates) across ages. Imaging results indicated that heightened VS activation during rewarded relative to neutral trials was specific to boyhood, post-obit a non-linear trajectory from childhood. Importantly, results also demonstrated rewards-enhanced activity in regions associated with oculomotor and inhibitory control in boyhood, providing farther insight on the possible processes underlying reward-modulated cognitive control during this developmental flow.

4.1. Rewards raise inhibitory command behavior

Consistent with previous developmental studies of inhibitory control (without an incentive) using the AS chore (Fischer et al., 1997, Klein and Foerster, 2001, Luna et al., 2004, Munoz et al., 1998), at that place were differences in operation in children and adolescents relative to adults on neutral trials. However, this was non observed in the advantage condition, where children and adolescents' performance increased to developed levels. This result suggests that younger participants have the ability to perform like adults when provided with an incentive to do so, reflecting a heightened relative motivation and a particular sensitivity to rewards.

Adults showed consistent inhibitory mistake rates (10–xx%) beyond incentives suggesting that their cognitive control is more stable and less decumbent to external influences and may already be optimal, at ceiling levels. However, similar to younger participants, adults showed faster latencies for correct rewarded AS trials relative to correct AS neutral trials supporting the notion that incentives influence the generation of voluntary saccades, consistent with previous work (Hikosaka et al., 2006, Geier et al., 2010). Developmental results are consequent with previous findings demonstrating improved cognitive performance and decreased latencies with the presentation of a monetary incentive in adolescents (Duka and Lupp, 1997, Geier et al., 2010, Hardin et al., 2007, Jazbec et al., 2005, Jazbec et al., 2006). The subtract in latencies and mistake rate during rewarded trials suggest optimization of behavior that leads to the receipt of a reward. Younger participants demonstrate that they improve functioning in tasks that take known immaturities within the context of a potential advantage, suggesting an enhancement in motivation that may be required to accomplish developed levels of performance. Similarly, immaturities in reward processing may enhance behaviors that appear to lead to a reward such as sensation seeking and adventure-taking, which can at times be suboptimal (Steinberg, 2004).

4.ii. Reward incentives enhance encephalon activity in adolescents

The encephalon regions supporting the generation of voluntary saccadic eye movements as well as the processing of rewards are well-delineated (Apicella et al., 1991, Breiter et al., 2001, Brownish et al., 2006, Delgado et al., 2000, Delgado et al., 2003, Elliott et al., 2003, Hikosaka and Watanabe, 2000, Knutson et al., 2000, Luna and Sweeney, 1999, Matsuda et al., 2004, Munoz and Everling, 2004, Roesch and Olson, 2003, Roesch and Olson, 2004, Schultz, 2000, Schultz et al., 2000, Thut et al., 1997). In the nowadays report, all three age groups robustly engaged key oculomotor control regions bilaterally across incentives including the FEF, SEF, inferior parietal sulcus (IPS), superior parietal lobule (SPL), putamen, and the dorsal ACC. Across ages, reward related regions were also recruited including VS, OFC and ACC. These results advise that the basic circuitry supporting inhibitory control and reward processing is in place by childhood.

Results indicated several age-related differences in the magnitude of recruitment of this circuitry suggesting unique developmental profiles of advantage processing and its influence on cognitive control in boyhood. Only adolescents showed a modulation of rewards on activity in right IPS, bilateral putamen, and bilateral VS. The IPS and putamen have both been associated with response planning, oculomotor command (Everling and Munoz, 2000), reward prediction (Peck et al., 2009) and outcome (Delgado et al., 2003). Increased activeness of these cardinal regions may support improved functioning during rewarded trials. The VS is a region that has been consistently associated with all phases of the processing of rewards, including detection, anticipation, and consequence (Bjork et al., 2004, Dreher et al., 2006, Galvan et al., 2006, Knutson et al., 2001, Schultz et al., 1992) and may underlie bias for firsthand over future rewards (McClure et al., 2004). In this region, nosotros observed a modulation of incentive condition in adolescents and a lack of differentiation by incentive type children and adults.

Age-related differences in incentive processing take been observed in other studies, with some studies demonstrating a relative under-activity during different stages of advantage processing such as cue detection (Geier et al., 2010) and reward anticipation (Bjork et al., 2004, Bjork et al., 2010) in VS and over-activity during advantage receipt (Ernst et al., 2005, van Leijenhorst et al., 2009, van Leijenhorst et al., 2010) and response grooming (Geier et al., 2010), likewise equally across an entire reward trial (Galvan et al., 2006). However, in our study, age-related differences were determined past the relative attenuated response to neutral trials in adolescents, a differentiation that was not nowadays in children and adults. Neutral trials in the context of an incentive task may be perceived as a relative loss of a advantage, rather than merely lacking in reward value. Furthermore, this relative difference between rewarded and neutral trials observed in adolescents may indicate an increased sensitivity to incentives that is non present in children or adults. DA neurons that heighten responses to reward contingencies in primary reward regions (such every bit VS), may contribute to enhanced signaling of oculomotor command neurons in regions such as the IPS, that may underlie enhanced performance. The IPS in particular has been establish to be involved in antisaccade preparation (Curtis and Connolly, 2008). Enhanced VS activity in the adolescent may result in increases in regions supporting the specific behavior that leads to rewards such every bit the IPS and its role in antisaccade performance (Brown et al., 2007, Curtis and Connolly, 2008).

Although children displayed the aforementioned behavioral design equally adolescents, their encephalon office in VS, putamen and IPS mimicked those of adults (i.e. did non differentiate past incentive condition). This finding is similar to other studies that demonstrated an "inverted U" in encephalon function across development, and highlights the peak in reward sensitivity in adolescence (Cohen et al., 2010, Somerville et al., 2010, van Leijenhorst et al., 2009, van Leijenhorst et al., 2010). Furthermore, children demonstrated increased activity in SEF for neutral trials and in the dorsal ACC for both advantage and neutral trials relative to the older groups. Increased reliance on oculomotor and prefrontal control regions during correct AS trails suggests that children may have relative increased difficulty in performing the antisaccade at optimal levels and may require greater date of critical regions to perform the task (Luna et al., 2001, Luna et al., 2004) diminishing potential differences between reward and neutral trials. Alternatively, children may accept recruited regions exterior of our a priori functionally divers brain regions to back up improve functioning in rewarded trials. Overall, children showed a distinct contour from boyhood and adulthood, reflecting dependence on medial prefrontal structures to perform the task regardless of incentives and not relying on oculomotor control or reward related regions to back up improved operation during rewarded trials.

Finally, similar to previous findings (Galvan et al., 2006, Geier et al., 2010, van Leijenhorst et al., 2009) merely adults recruited the OFC during rewarded trials. The lateral OFC has been previously implicated in many aspects of advantage processing especially in coding representations of valence and magnitude of reward and penalty and is highly continued to the basal ganglia (Breiter et al., 2001, Delgado et al., 2000, Hikosaka and Watanabe, 2000, Knutson et al., 2000, O'Doherty et al., 2004, Roesch and Olson, 2003, Roesch and Olson, 2004, Schultz et al., 2000, Wise, 2002). The OFC may support the executive processing of rewards. This more executive component of reward processing may nonetheless exist young in boyhood.

Relative increased sensitivity in the VS coupled with under-activity of the OFC in response to rewards in adolescence may result in a vulnerability to behavior that is directed by incentives when executive value has not been properly assessed. The unique circuitry recruited by adolescents may exist associated with the known structural immaturities including continued grey matter thinning of the basal ganglia (Sowell et al., 2002) and OFC (Gogtay et al., 2004), and increases in dopamine manual (Kalsbeek et al., 1988, Meng et al., 1999, Rosenberg and Lewis, 1994, Rosenberg and Lewis, 1995, Seeman et al., 1987). This may heighten reward furnishings and undermine the executive assessment of rewards. Adventure-taking involves behavior that is guided by reward receipt with limitations in executive aspects of reward value and consequences. In this manner, these results suggest that the circuitry that supports executive assessment of rewards and modulation of motivation may all the same be immature in adolescence and contribute to the high rate of adventure-taking in boyhood. That is, adolescents may be more than influenced by limbic system control, which could override their power to effectively use executive control systems (Spear, 2000).

four.3. Limitations

We annotation limitations in the present study in society to inform time to come studies. Our sample size of 10 participants per age group limited our power to appraise pubertal status, sex, and continuous age effects. With our present sample size we had the ability to detect medium to large effects with iii-way (Age Group by Condition by Fourth dimension) and a 2 manner interactions (Historic period Group by Condition) (effect size: .201). We besides annotation that this limitation in power indicates that there may be even more historic period related differences than the ones reported in the present study, especially with regards to the pocket-sized differences constitute in the kid grouping. On the other paw, our power indicates that our findings regarding functional differences in boyish brain function is a robust event. Furthermore, this written report used monetary incentives as an index of reward. It is not clear whether the incentive was considered "equal" across historic period groups. Future studies in our laboratory focus on equating incentives to improve assess developmental effects.

v. Decision

Overall, our results speak to a key component of adolescent immaturity, which lies in the differences in motivationally driven behaviors. A motivated behavior refers to the ability of an organism to designate a motor output based on the value it places on a stimulus input (which is based on learned associations or prior experience with the stimulus), thereby interim to approach or avert the stimulus (Ernst et al., 2009, Salamone and Correa, 2002). Critical to motivated behaviors are the brain systems (perceptual, cognitive, emotional) that allow for the processing of external cues or internal brain states, allowing for an optimal response to be made. Our results that adolescents showed increased action in regions supporting performance that resulted in reward receipt reflect enhancements in motivation. It is possible that younger individuals crave this added motivation to perform the chore at optimal levels.

The current findings advise that basic neural circuitry underlying response inhibition and incentive processing is established in childhood. Nonetheless, immaturities in regions associated with advantage reactivity and executive assessment appear to follow a non-linear developmental trajectory from babyhood through boyhood into adulthood. Adolescents showed reward related increases in reward and cognitive command related regions while showing limitations in executive cess of rewards. Our results support current models regarding adolescent immaturities in reward processing and cognitive control, suggesting that an overall over-reactive advantage response may enhance engaging in behaviors that result in firsthand rewards. Taken together, these findings betoken immaturities in the developing brain that could be particularly vulnerable to risk taking and other suboptimal behaviors during adolescence.

Futurity investigations into the nature of motivated behaviors in adolescence should examine other types of incentives (i.e. social), that likely play a large role in determining behavior.

Grant

This study was supported by National Constitute of Mental Wellness Grant MH080243.

Acknowledgements

We give thanks Robert Terwilliger for advice related to the methods and analysis conducted in this manuscript. We besides thank Emi Yasui, Natalie Nawarawong and Alina Vaisleib for assistance with information collection and scoring of eye data. We also thank all participants and their families who volunteered for this study.

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Source: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3181104/

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