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Abnormal striatal BOLD responses to reward anticipation and reward delivery in ADHD.

Furukawa E, Bado P, Tripp G, Mattos P, Wickens JR, Bramati IE, Alsop B, Ferreira FM, Lima D, Tovar-Moll F, Sergeant JA, Moll J - PLoS ONE (2014)

Bottom Line: The neurobiological mechanism underlying this alteration remains unclear.Data from 14 high-functioning and stimulant-naïve young adults with elevated lifetime symptoms of ADHD (8 males, 6 females) and 15 well-matched controls (8 males, 7 females) were included in the analyses.The opposite pattern was observed in response to reward delivery; the ADHD group demonstrated significantly greater BOLD responses in the ventral striatum bilaterally and the left dorsal striatum relative to controls.

View Article: PubMed Central - PubMed

Affiliation: Okinawa Institute of Science and Technology Graduate University (OIST), Okinawa, Japan.

ABSTRACT
Altered reward processing has been proposed to contribute to the symptoms of attention deficit hyperactivity disorder (ADHD). The neurobiological mechanism underlying this alteration remains unclear. We hypothesize that the transfer of dopamine release from reward to reward-predicting cues, as normally observed in animal studies, may be deficient in ADHD. Functional magnetic resonance imaging (fMRI) was used to investigate striatal responses to reward-predicting cues and reward delivery in a classical conditioning paradigm. Data from 14 high-functioning and stimulant-naïve young adults with elevated lifetime symptoms of ADHD (8 males, 6 females) and 15 well-matched controls (8 males, 7 females) were included in the analyses. During reward anticipation, increased blood-oxygen-level-dependent (BOLD) responses in the right ventral and left dorsal striatum were observed in controls, but not in the ADHD group. The opposite pattern was observed in response to reward delivery; the ADHD group demonstrated significantly greater BOLD responses in the ventral striatum bilaterally and the left dorsal striatum relative to controls. In the ADHD group, the number of current hyperactivity/impulsivity symptoms was inversely related to ventral striatal responses during reward anticipation and positively associated with responses to reward. The BOLD response patterns observed in the striatum are consistent with impaired predictive dopamine signaling in ADHD, which may explain altered reward-contingent behaviors and symptoms of ADHD.

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Striatal responses to reward anticipation and reward delivery in the ADHD and control groups.Brain activation displays were generated by overlaying SPM t-maps resulting from the group-level analyses on an MNI standard brain (p<.005 uncorrected, cluster size ≥5 voxel, for visualization purposes) and applying a gray matter mask. (A) Increased activation in the left dorsal striatum (head of caudate) and right ventral striatum (nucleus accumbens and ventral putamen) during reward anticipation in the control group. (B) Increased activation in the left dorsal striatum (head of caudate), left ventral striatum (ventral regions of the head of caudate), and right ventral striatum (nucleus accumbens and ventral putamen) in response to reward delivery in ADHD. (C) Bar graphs represent mean parameter estimates and standard errors from the GLM analyses examining the effects of reward anticipation (Cue A delay – Cue B delay contrast) and reward delivery (Cue A reward – Cue B non-reward contrast), which were extracted from the local maxima observed within the a priori-defined ROIs based on a meta-analysis (Liu et al., 2011); MNI x, y, z = 18, 17, −5 for rVS, −15, 8, 16 for lDS in response to reward anticipation; MNI x, y, z = 9, 17, −11 for rVS, −9, 17, 1 for lVS, −18, 8, 16 for lDS in response to reward delivery. These graphs are provided for illustrative purposes only, and were not used for statistical inferences.
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pone-0089129-g002: Striatal responses to reward anticipation and reward delivery in the ADHD and control groups.Brain activation displays were generated by overlaying SPM t-maps resulting from the group-level analyses on an MNI standard brain (p<.005 uncorrected, cluster size ≥5 voxel, for visualization purposes) and applying a gray matter mask. (A) Increased activation in the left dorsal striatum (head of caudate) and right ventral striatum (nucleus accumbens and ventral putamen) during reward anticipation in the control group. (B) Increased activation in the left dorsal striatum (head of caudate), left ventral striatum (ventral regions of the head of caudate), and right ventral striatum (nucleus accumbens and ventral putamen) in response to reward delivery in ADHD. (C) Bar graphs represent mean parameter estimates and standard errors from the GLM analyses examining the effects of reward anticipation (Cue A delay – Cue B delay contrast) and reward delivery (Cue A reward – Cue B non-reward contrast), which were extracted from the local maxima observed within the a priori-defined ROIs based on a meta-analysis (Liu et al., 2011); MNI x, y, z = 18, 17, −5 for rVS, −15, 8, 16 for lDS in response to reward anticipation; MNI x, y, z = 9, 17, −11 for rVS, −9, 17, 1 for lVS, −18, 8, 16 for lDS in response to reward delivery. These graphs are provided for illustrative purposes only, and were not used for statistical inferences.

Mentions: Within-group analyses revealed increased BOLD responses in right ventral striatum (rVS) and left dorsal striatum (lDS) in the control group during reward anticipation (Cue A delay – Cue B delay) (Figure 2, Table 1). In contrast, consistent with our predictions, there were no statistically significant hemodynamic effects during reward anticipation in the ADHD group. Between-group comparisons (Control – ADHD) indicated significantly greater responses in rVS and lDS in the controls, compared to the ADHD group.


Abnormal striatal BOLD responses to reward anticipation and reward delivery in ADHD.

Furukawa E, Bado P, Tripp G, Mattos P, Wickens JR, Bramati IE, Alsop B, Ferreira FM, Lima D, Tovar-Moll F, Sergeant JA, Moll J - PLoS ONE (2014)

Striatal responses to reward anticipation and reward delivery in the ADHD and control groups.Brain activation displays were generated by overlaying SPM t-maps resulting from the group-level analyses on an MNI standard brain (p<.005 uncorrected, cluster size ≥5 voxel, for visualization purposes) and applying a gray matter mask. (A) Increased activation in the left dorsal striatum (head of caudate) and right ventral striatum (nucleus accumbens and ventral putamen) during reward anticipation in the control group. (B) Increased activation in the left dorsal striatum (head of caudate), left ventral striatum (ventral regions of the head of caudate), and right ventral striatum (nucleus accumbens and ventral putamen) in response to reward delivery in ADHD. (C) Bar graphs represent mean parameter estimates and standard errors from the GLM analyses examining the effects of reward anticipation (Cue A delay – Cue B delay contrast) and reward delivery (Cue A reward – Cue B non-reward contrast), which were extracted from the local maxima observed within the a priori-defined ROIs based on a meta-analysis (Liu et al., 2011); MNI x, y, z = 18, 17, −5 for rVS, −15, 8, 16 for lDS in response to reward anticipation; MNI x, y, z = 9, 17, −11 for rVS, −9, 17, 1 for lVS, −18, 8, 16 for lDS in response to reward delivery. These graphs are provided for illustrative purposes only, and were not used for statistical inferences.
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC3935853&req=5

pone-0089129-g002: Striatal responses to reward anticipation and reward delivery in the ADHD and control groups.Brain activation displays were generated by overlaying SPM t-maps resulting from the group-level analyses on an MNI standard brain (p<.005 uncorrected, cluster size ≥5 voxel, for visualization purposes) and applying a gray matter mask. (A) Increased activation in the left dorsal striatum (head of caudate) and right ventral striatum (nucleus accumbens and ventral putamen) during reward anticipation in the control group. (B) Increased activation in the left dorsal striatum (head of caudate), left ventral striatum (ventral regions of the head of caudate), and right ventral striatum (nucleus accumbens and ventral putamen) in response to reward delivery in ADHD. (C) Bar graphs represent mean parameter estimates and standard errors from the GLM analyses examining the effects of reward anticipation (Cue A delay – Cue B delay contrast) and reward delivery (Cue A reward – Cue B non-reward contrast), which were extracted from the local maxima observed within the a priori-defined ROIs based on a meta-analysis (Liu et al., 2011); MNI x, y, z = 18, 17, −5 for rVS, −15, 8, 16 for lDS in response to reward anticipation; MNI x, y, z = 9, 17, −11 for rVS, −9, 17, 1 for lVS, −18, 8, 16 for lDS in response to reward delivery. These graphs are provided for illustrative purposes only, and were not used for statistical inferences.
Mentions: Within-group analyses revealed increased BOLD responses in right ventral striatum (rVS) and left dorsal striatum (lDS) in the control group during reward anticipation (Cue A delay – Cue B delay) (Figure 2, Table 1). In contrast, consistent with our predictions, there were no statistically significant hemodynamic effects during reward anticipation in the ADHD group. Between-group comparisons (Control – ADHD) indicated significantly greater responses in rVS and lDS in the controls, compared to the ADHD group.

Bottom Line: The neurobiological mechanism underlying this alteration remains unclear.Data from 14 high-functioning and stimulant-naïve young adults with elevated lifetime symptoms of ADHD (8 males, 6 females) and 15 well-matched controls (8 males, 7 females) were included in the analyses.The opposite pattern was observed in response to reward delivery; the ADHD group demonstrated significantly greater BOLD responses in the ventral striatum bilaterally and the left dorsal striatum relative to controls.

View Article: PubMed Central - PubMed

Affiliation: Okinawa Institute of Science and Technology Graduate University (OIST), Okinawa, Japan.

ABSTRACT
Altered reward processing has been proposed to contribute to the symptoms of attention deficit hyperactivity disorder (ADHD). The neurobiological mechanism underlying this alteration remains unclear. We hypothesize that the transfer of dopamine release from reward to reward-predicting cues, as normally observed in animal studies, may be deficient in ADHD. Functional magnetic resonance imaging (fMRI) was used to investigate striatal responses to reward-predicting cues and reward delivery in a classical conditioning paradigm. Data from 14 high-functioning and stimulant-naïve young adults with elevated lifetime symptoms of ADHD (8 males, 6 females) and 15 well-matched controls (8 males, 7 females) were included in the analyses. During reward anticipation, increased blood-oxygen-level-dependent (BOLD) responses in the right ventral and left dorsal striatum were observed in controls, but not in the ADHD group. The opposite pattern was observed in response to reward delivery; the ADHD group demonstrated significantly greater BOLD responses in the ventral striatum bilaterally and the left dorsal striatum relative to controls. In the ADHD group, the number of current hyperactivity/impulsivity symptoms was inversely related to ventral striatal responses during reward anticipation and positively associated with responses to reward. The BOLD response patterns observed in the striatum are consistent with impaired predictive dopamine signaling in ADHD, which may explain altered reward-contingent behaviors and symptoms of ADHD.

Show MeSH
Related in: MedlinePlus